July 09, 2009

Climate has driven mtDNA variation in humans

Yann Klimentidis points me to this very exciting new paper. Some of its authors also contributed to another recent paper which investigated the role of climate in shaping human cranial variation.

The authors compared autosomal, X chromosome and Y chromosome genetic variation with that of mtDNA. For example an impressive 85% of autosomal microsatellite diversity in worldwide humans can be explained by their distance from Africa, but no apparent effect is seen for climate. The effect of distance from Africa is only 18% for HVS-I of human mtDNA, and a strong effect of climate measures (such as temperature) is seen. On the contrary, human Y chromosomes show no relationship with climate.

The effect of climate is also resilient to accounting for distance from Africa (which is very hot, and thus distance from it might be expected to correlate with a decrease in temperature; it is not), and by removing populations living in extreme arctic conditions, for which thermoregulation is of the utmost importance.

I would say that this paper represents the best evidence so far of selection acting on the human Y chromosome.

The implications of this are manifold, and they relate:

(i) to the use of mtDNA to assess population relationships. For example, South Asians have a strong affinity with West Eurasians in their Y-chromosomes and with East Asians in their mtDNA. Nonetheless they do not occupy an intermediate position between the two in autosomal DNA, but are predominantly aligned to West Eurasians.

(ii) to the overall mitochondrial time depth of humanity, i.e., the age of mitochondrial Eve, and what that implies about the recentness of our species (it may be older than its mtDNA time depth), and its possible admixture with other human populations such as Neandertals (it may have occurred, but the non-modern mtDNA may have been selected against)

(iii) to the potential of solving, at least in part, discrepancies between present-day and archaeological mtDNA gene pools, which may not in fact reflect processes of migration, but climate shifts over time.

Note that this is not the first time that adaptive evolution of human mtDNA has been proposed. For example five years ago, Ruiz-Pesini et al. noticed the conservation of internal branch amino acid substitutions at high latitudes, and made the case for energy-related climate adaptation in human mtDNA. The current paper makes a different argument, but arrives at a similar conclusion.

There is an ongoing discussion in the literature on whether human mitochondrial DNA (mtDNA) evolves neutrally. There have been previous claims for natural selection on human mtDNA based on an excess of non-synonymous mutations and higher evolutionary persistence of specific mitochondrial mutations in Arctic populations. However, these findings were not supported by the reanalysis of larger datasets. Using a geographical framework, we perform the first direct test of the relative extent to which climate and past demography have shaped the current spatial distribution of mtDNA sequences worldwide. We show that populations living in colder environments have lower mitochondrial diversity and that the genetic differentiation between pairs of populations correlates with difference in temperature. These associations were unique to mtDNA; we could not find a similar pattern in any other genetic marker. We were able to identify two correlated non-synonymous point mutations in the ND3 and ATP6 genes characterized by a clear association with temperature, which appear to be plausible targets of natural selection producing the association with climate. The same mutations have been previously shown to be associated with variation in mitochondrial pH and calcium dynamics. Our results indicate that natural selection mediated by climate has contributed to shape the current distribution of mtDNA sequences in humans.

9 comments:

As I was just typing at Anthropology.net, figure 4 makes things look not clear at all: the Oceanian and European clusters have same frequency for these two loci and they have very different tempaeratures. Oceanians should cluster with Tropical Africans instead but they don't: they cluster with Europeans. Similarly the main Asian clusters have the same temperature as the main European cluster and they have very different frequencies for both loci.

Will have to read this one when I get back to the lab, but a note. The Ruiz-Pesini et al study has shown itself not to be reproducible when you use any other collection of mtDNA sequences (of the same haplogroups). Their observations may be due to their specific sub-sampled sequence set.

“(i) to the use of mtDNA to assess population relationships. For example, South Asians have a strong affinity with West Eurasians in their Y-chromosomes and with East Asians in their mtDNA. Nonetheless they do not occupy an intermediate position between the two in autosomal DNA, but are predominantly aligned to West Eurasians.”

What affinity does South Asian mtDNA have with East Asian mtDNA? Affinity with East Asian can only be based on the proportions of D, G, M7-M9, A, N9, R9, B. which non admixed South Asian populations don’t have.

I'd say that, if anything, South Asians relate more clearly mtDNA-wise with West Eurasians too. At least they do share some real haplogroups like U, N2 (and its derived form W), R2'J, N1'5 and probably also others.

There are no or very few similar level mtDNA lineages shared between East and South Asians.

You are confusing admixture with affinity. The great majority of Indian mtDNA has a closer affinity to that of East Asians than it does with that of West Eurasians, as it belongs to macrohaplogroup M.

Similarly, Nigerians and Ainus have a greater affinity in their Y-chromosomes than Ainus have with the Chinese, as they both belong to haplogroup DE. The fact that the two belong to disjoint clades of DE does not negate their greater affinity.

The typical South Asian mitochondrion has fewer generations separating it from the typical Chinese mitochondrion than it does with a European mitochondrion.

Well, IMO you're deducing too much of macrohaplogroups. I'd pay more attention to more derived lineages personally, which do show clear connections (albeit not as strong as Y-DNA) between West and South Eurasia and not between South and East Asia.

That macrohaplo M, and to a large extent also macrohaplo N(xR), participated only at low levels in the colonization of West Eurasia (2 and 3 lineages respectively) to me only means that the wave heading west was mostly mtDNA R from the beginning.

“You are confusing admixture with affinity. The great majority of Indian mtDNA has a closer affinity to that of East Asians than it does with that of West Eurasians, as it belongs to macrohaplogroup M.

Similarly, Nigerians and Ainus have a greater affinity in their Y-chromosomes than Ainus have with the Chinese, as they both belong to haplogroup DE. The fact that the two belong to disjoint clades of DE does not negate their greater affinity.

The typical South Asian mitochondrion has fewer generations separating it from the typical Chinese mitochondrion than it does with a European mitochondrion.”

Clade affinity of M and N may not represent real population affinity. M and N clades diverged from L3 after 74kyr but did the population? If you assume an isolated Proto-Eurasian population carrying {M, N,R} and {F,C,K} shortly before expanding 55kyr then there is no greater population affinity between West/East/South Eurasians populations based on M and N relationship right?

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